[en] Sleep loss affects human behavior in a nonuniform manner, depending on the cognitive domain and also the circadian phase. Besides, evidence exists about stable interindividual variations in sleep loss-related performance impairments. Despite this evidence, only a few studies have considered both circadian phase and neurobehavioral domain when investigating trait-like vulnerability to sleep manipulation. By applying a randomized, crossover design with 2 sleep pressure conditions (40 h sleep deprivation vs. 40 h multiple naps), we investigated the influence of a human adenosine deaminase (ADA) polymorphism (rs73598374) on several behavioral measures throughout nearly 2 circadian cycles. Confirming earlier studies, we observed that under sleep deprivation the previously reported vulnerable G/A-allele carriers felt overall sleepier than G/G-allele carriers. As expected, this difference was no longer present when sleep pressure was reduced by the application of multiple naps. Concomitantly, well-being was worse in the G/A genotype under sleep loss when compared to the nap protocol, and n-back working memory performance appeared to be specifically susceptible to sleep-wake manipulation in this genotype. When considering psychomotor vigilance performance, however, a higher sensitivity to sleep-wake manipulation was detected in homozygous participants, but specifically at the end of the night and only for optimal task performance. Although these data are based on a small sample size and hence require replication (12 G/A- and 12 G/G-allele carriers), they confirm the assumption that interindividual differences regarding the effect of sleep manipulation highly depend on the cognitive task and circadian phase, and thus emphasize the necessity of a multimethodological approach. Moreover, they indicate that napping might be suitable to counteract endogenously heightened sleep pressure depending on the neurobehavioral domain.
Disciplines :
Neurosciences & behavior
Author, co-author :
Reichert, Carolin F.
Maire, Micheline
Gabel, Virginie
Viola, Antoine U.
Kolodyazhniy, Vitaliy
Strobel, Werner
Gotz, Thomas
Bachmann, Valerie
Landolt, Hans-Peter
Cajochen, Christian
Schmidt, Christina ; Université de Liège > Département de Psychologie : cognition et comportement > Neuropsychologie
Language :
English
Title :
Insights into behavioral vulnerability to differential sleep pressure and circadian phase from a functional ADA polymorphism.
Akerstedt T, Gillberg M. Subjective and objective sleepiness in the active individual. Int J Neurosci. 1990 ; 52: 29-37
Bachmann V, Klaus F, Bodenmann S, Schafer N, Brugger P, Huber S, et al. Functional ADA polymorphism increases sleep depth and reduces vigilant attention in humans. Cereb Cortex. 2012 ; 22: 962-970
Basner M, Dinges DF. Maximizing sensitivity of the psychomotor vigilance test (PVT) to sleep loss. Sleep. 2011 ; 34: 581-591
Battistuzzi G, Iudicone P, Santolamazza P, Petrucci R. Activity of adenosine deaminase allelic forms in intact erythrocytes and in lymphocytes. Ann Hum Genet. 1981 ; 45: 15-19
Birchler-Pedross A, Schroder CM, Munch M, Knoblauch V, Blatter K, Schnitzler-Sack C, et al. Subjective well-being is modulated by circadian phase, sleep pressure, age, and gender. J Biol Rhythms. 2009 ; 24: 232-242
Bromundt V, Frey S, Odermatt J, Cajochen C. Extraocular light via the ear canal does not acutely affect human circadian physiology, alertness and psychomotor vigilance performance. Chronobiol Int. 2013 ;:
Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989 ; 28: 193-213
Cajochen C, Dijk DJ. Electroencephalographic activity during wakefulness, rapid eye movement and non-rapid eye movement sleep in humans: comparison of their circadian and homeostatic modulation. Sleep Biol Rhythms. 2003 ; 1: 85-95
Cajochen C, Knoblauch V, Krauchi K, Renz C, Wirz-Justice A. Dynamics of frontal EEG activity, sleepiness and body temperature under high and low sleep pressure. Neuroreport. 2001 ; 12: 2277-2281
Chee MW, Chuah LY. Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition. Curr Opin Neurol. 2008 ; 21: 417-423
Cohen DA, Wang W, Wyatt JK, Kronauer RE, Dijk DJ, Czeisler CA, et al. Uncovering residual effects of chronic sleep loss on human performance. Sci Transl Med. 2010 ; 2: 14-13
Curran-Everett D. Multiple comparisons: philosophies and illustrations. Am J Physiol Regul Integr Comp Physiol. 2000 ; 279: R1 - R8
Danilenko KV, Cajochen C, Wirz-Justice A. Is sleep per se a zeitgeber in humans?. J Biol Rhythms. 2003 ; 18: 170-178
Dijk DJ, Duffy JF, Czeisler CA. Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J Sleep Res. 1992 ; 1: 112-117
Dinges DF, Powell JW. Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behav Res Meth Instr Comp. 1985 ; 17: 625-655
Drummond SP, Bischoff-Grethe A, Dinges DF, Ayalon L, Mednick SC, Meloy MJ. The neural basis of the psychomotor vigilance task. Sleep. 2005 ; 28: 1059-1068
Duffy JF, Wright KP. Entrainment of the human circadian system by light. J Biol Rhythms. 2005 ; 20: 326-338
Escames G, Ozturk G, Bano-Otalora B, Pozo MJ, Madrid JA, Reiter RJ, et al. Exercise and melatonin in humans: reciprocal benefits. J Pineal Res. 2012 ; 52: 1-11
Feillet CA. Food for thoughts: feeding time and hormonal secretion. J Neuroendocrinol. 2010 ; 22: 620-628
Franken P, Chollet D, Tafti M. The homeostatic regulation of sleep need is under genetic control. J Neurosci. 2001 ; 21: 2610-2621
Horne JA, Östberg O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Intl J Chronobiol. 1976 ; 4: 97-110
Jaeggi SM, Buschkuehl M, Perrig WJ, Meier B. The concurrent validity of the N-back task as a working memory measure. Memory. 2010 ; 18: 394-412
Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991 ; 14: 540-545
Kane MJ, Conway AR, Miura TK, Colflesh GJ. Working memory, attention control, and the n-back task: a question of construct validity. J Exp Psychol Learn Mem Cogn. 2007 ; 33: 615-622
Kenward MG, Roger JH. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics. 1997 ; 53: 983-997
King AC, Belenky G, Van Dongen HP. Performance impairment consequent to sleep loss: determinants of resistance and susceptibility. Curr Opin Pulm Med. 2009 ; 15: 559-564
Knoblauch V, Krauchi K, Renz C, Wirz-Justice A, Cajochen C. Homeostatic control of slow-wave and spindle frequency activity during human sleep: effect of differential sleep pressure and brain topography. Cereb Cortex. 2002 ; 12: 1092-1100
Kolodyazhniy V, Späti J, Frey S, Gotz T, Wirz-Justice A, Krauchi K, et al. An improved method for estimating human circadian phase derived from multichannel ambulatory monitoring and artificial neural networks. Chronobiol Intl. 2012 ; 29: 1078-1097
Kuna ST, Maislin G, Pack FM, Staley B, Hachadoorian R, Coccaro EF, et al. Heritability of performance deficit accumulation during acute sleep deprivation in twins. Sleep. 2012 ; 35: 1223-1233
Kuriyama K, Mishima K, Suzuki H, Aritake S, Uchiyama M. Sleep accelerates the improvement in working memory performance. J Neurosci. 2008 ; 28: 10145-10150
Landolt HP. Sleep homeostasis: a role for adenosine in humans?. Biochem Pharmacol. 2008 ; 75: 2070-2079
Landolt HP. Genetic determination of sleep EEG profiles in healthy humans. Prog Brain Res. 2011 ; 193: 51-61
Lewy AJ, Sack RL. The dim light melatonin onset as a marker for circadian phase position. Chronobiol Int. 1989 ; 6: 93-102
Lim J, Dinges DF. Sleep deprivation and vigilant attention. Ann N Y Acad Sci. 2008 ; 1129: 305-322
Lo JC, Groeger JA, Santhi N, Arbon EL, Lazar AS, Hasan S, et al. Effects of partial and acute total sleep deprivation on performance across cognitive domains, individuals and circadian phase. PLoS One. 2012 ; 7: e45987
Maire M, Reichert C, Schmidt C. Current and future perspectives in sleep and circadian rhythms research. J Cogn Behav Psychother forthcoming. 2014 ;:
Mazzotti DR, Guindalini C, de Souza AA, Sato JR, Santos-Silva R, Bittencourt LR, et al. Adenosine deaminase polymorphism affects sleep EEG spectral power in a large epidemiological sample. PLoS One. 2012 ; 7: e44154
Naitoh P, Kelly T, Babkoff H. Sleep inertia: best time not to wake up?. Chronobiol Intl. 1993 ; 10: 109-118
Porkka-Heiskanen T, Kalinchuk AV. Adenosine, energy metabolism and sleep homeostasis. Sleep Med Rev. 2011 ; 15: 123-135
Retey JV, Adam M, Honegger E, Khatami R, Luhmann UF, Jung HH, et al. A functional genetic variation of adenosine deaminase affects the duration and intensity of deep sleep in humans. Proc Natl Acad Sci U S A. 2005 ; 102: 15676-15681
Riksen NP, Franke B, van den Broek P, Naber M, Smits P, Rongen GA. The 22G>A polymorphism in the adenosine deaminase gene impairs catalytic function but does not affect reactive hyperaemia in humans in vivo. Pharmacogenet Genomics. 2008 ; 18: 843-846
Roenneberg T, Wirz-Justice A, Merrow M.. Life between clocks: daily temporal patterns of human chronotypes. J Biol Rhythms. 2003 ; 18: 80-90
Sagaspe P, Taillard J, Amieva H, Beck A, Rascol O, Dartigues JF, et al. Influence of age, circadian and homeostatic processes on inhibitory motor control: a Go/Nogo task study. PLoS One. 2012 ; 7: e39410
Schmidt C, Collette F, Cajochen C, Peigneux P. A time to think: circadian rhythms in human cognition. Cogn Neuropsychol. 2007 ; 24: 755-789
Schmidt C, Collette F, Leclercq Y, Sterpenich V, Vandewalle G, Berthomier P, et al. Homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area. Science. 2009 ; 324: 516-519
Scullin MK, Trotti LM, Wilson AG, Greer SA, Bliwise DL. Nocturnal sleep enhances working memory training in Parkinson's disease but not Lewy body dementia. Brain. 2012 ; 135: 2789-2797
Steenari MR, Vuontela V, Paavonen EJ, Carlson S, Fjallberg M, Aronen E. Working memory and sleep in 6- to 13-year-old schoolchildren. J Am Acad Child Adolesc Psychiatry. 2003 ; 42: 85-92
Tassi P, Muzet A. Sleep inertia. Sleep Med Rev. 2000 ; 4: 341-353
Vandewalle G, Archer SN, Wuillaume C, Balteau E, Degueldre C, Luxen A, et al. Functional magnetic resonance imaging-assessed brain responses during an executive task depend on interaction of sleep homeostasis, circadian phase, and PER3 genotype. J Neurosci. 2009 ; 29: 7948-7956
Van Dongen HP, Baynard MD, Maislin G, Dinges DF. Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. Sleep. 2004 ; 27: 423-433
Van Dongen HP, Bender AM, Dinges DF. Systematic individual differences in sleep homeostatic and circadian rhythm contributions to neurobehavioral impairment during sleep deprivation. Accid Anal Prev. 2012 ; 45: 11-16
Viola AU, Archer SN, James LM, Groeger JA, Lo JC, Skene DJ, von Schantz M, Dijk DJ. PER3 polymorphism predicts sleep structure and waking performance. Curr Biol. 2007 ; 17: 613-618
Wyatt JK, Dijk DJ, Ritz-de Cecco A, Ronda JM, Czeisler CA. Sleep-facilitating effect of exogenous melatonin in healthy young men and women is circadian-phase dependent. Sleep. 2006 ; 29: 609-618
Wyatt JK, Ritz-De Cecco A, Czeisler CA, Dijk DJ. Circadian temperature and melatonin rhythms, sleep, and neurobehavioral function in humans living on a 20-h day. Am J Physiol. 1999 ; 277: R1152 - R1163
Zeitzer JM, Dijk DJ, Kronauer R, Brown E, Czeisler C. Sensitivity of the human circadian pacemaker to nocturnal light: melatonin phase resetting and suppression. J Physiol. 2000 ; 526 (Pt. 3). 695-702